A Devil Indeed

The Tasmanian devil (Sarcophilus harrisii) is a carnivorous marsupial found in the wild only in the Australian island state of Tasmania. After the extinction in 1936 of the Tasmanian tiger (or Thylacine), another well-known carnivorous marsupial, the Tasmanian devil became the largest carnivorous marsupial in the world. They received their common name from the first European settlers, who called them “devils” when they encountered a fierce, noisy creature with large teeth, a “bad-temper”, and a habit of growling, yelling and screaming when annoyed, and which was always around at night. However, unlike the meaning of its name, young Tasmanian devils are cute, playful and easily tamed. Even adult Tasmanian devils are somewhat undeserving of their nickname. When startled they can put on spectacular displays of aggression in which they produce a variety of fierce noises, from harsh coughs and snarls to high pitched screeches (the famous “demonic” growling). However, this is actually a bluff; Tasmanian devils are not threatening fighters and can be easily overcome by the average farm dog. Since they generally avoid human contact and can be dangerous when startled or handled, the Tasmanian devil was once incorrectly perceived as a destructive creature. However, more recently Tasmanian devils have been recognised as a useful wildlife species. The presence of devils benefits farmers, and the species has many important roles in the natural ecosystem. The Tasmanian devil has recently been listed as endangered and faces the threat of extinction due to an unusual and devastating disease.

Physically, the Tasmanian devil appears like a small and stocky, thick-haired black dog, often with distinctive patches of white fur on their chest or rump. They are carnivorous scavengers, and their main diet consists of dead animals. Sometimes but rarely, they hunt other wild or domestic animals, such as wombats, birds, fish and even sheep. They do not prey on any other species in particular. While devils are usually solitary creatures, they often feed co-operatively with a number of other devils on a single piece of carrion, during a session of raucous communal eating that can be heard a mile away. There is little trace of a carcass after Tasmanian devils finish eating. Tasmanian devils are nocturnal, and seldom seen in daylight.

The Plight of the Devil

Approximately 600 years ago, the devil went extinct on Australia’s mainland, which is thought to be due to its predation by dingoes and indigenous Australians. This left the island of Tasmania as this animal’s only refuge. However, life in Tasmania has not been trouble-free for the devils. Their population has suffered several crashes due to human extermination efforts (circa 1830-1930) and two other population crashes in 1909 and 1950, which are thought to be due to disease epidemics. After the extinction of the Tasmanian Tiger in 1936, laws were passed to protect the Tasmanian Devil in 1941, allowing the population to slowly recover, causing their conservation status to be amended to the lowest risk. As a result of Devil Facial Tumour Disease (DFTD), which is caused by an infectious tumor that was first obseved in 1996, the conservation status of the Tasmanian devil changed from vulnerable to endangered in 2009. Since the recognition of this disease, the number of devil sightings has decreased by an average of 90% with an estimated population decline of 50% since 1996. This disease kills more than 90% and 40-50% of adults in high and medium density populations, respectively, and has spread across more than 65% of the island state. Some epidemiologists have reported that, without intervention, the Tasmanian Devil’s could become functionally extinct by 2024. Therefore, on May 2009, Tasmanian devils were reclassified as endangered by the Australian Environment Protection and Biodiversity Conservation Act 1999.

Yep, an Infectious Tumour

Devil Facial Tumour Disease (DFTD) is characterized by tumour formation surrounding the face and neck, which interferes with feeding and causes death via starvation in 12-18 months after contraction. DFTD is thought to be spread when animals bite each other during feeding or mating sessions. The cancer cells themselves are the infective agent, as opposed to a transmissible virus that leads to tumour formation. Normally, a host can recognize foreign cells as ‘non-self’ and eliminate them, making transmissible cancers very rare. However, in the case of the devils, the genes involved in differentiating between ‘self’ and ‘non-self’ are so similar between the cancer and host, that the cancer is not recognized by the devil’s immune system, allowing it to grow into a tumour uncontrollably. Complicating the issue is that the level of genetic diversity between devils is extremely low, meaning that the cancer can spread between most all Tasmanian Devils without rejection.

The two-parted story behind DFTD

Part 1. The Cancer. When there is a sudden epidemic of cancer, one of a few causes is usually behind the increased disease prevalence: environmental factors such as mutagens and carcinogens, or, transmission of an infectious agent that causes cancer formation. In the case of DFTD, environmental factors were ruled out rather quickly, leading researchers to assume that transmission of a pathogen, such as a virus, was the underlying cause of this cancer. However, no such agent could be identified, leaving researchers stumped. Although extremely rare, a few cases of transmissible cancers (e.g. when the cancer cell itself is the infectious agent and not a virus) have been identified. To determine if a transmissible cancer may indeed cause DFTD, the tumors from 11 devils presenting with DFTD were examined. The tumors from every animal had the same genetic arrangement, which was dramatically different from the normal genetic arrangement of all non-tumor cells. Since the chromosomal arrangement was so highly similar between tumor cells and was extremely rearranged compared to normal cells, it was concluded that DFTD was transmitted by the cancerous cells themselves (primary research article).

Part 2. The Transmission. Nearly all cancers are caused by genetic abnormalities in a cell, which results in an uncontrolled outgrowth. These outgrowths are derived from the host’s own cells, meaning that the host’s immune system recognizes the growth a ‘self,’ leaving the cells to grow uncontrollably. If these cancer cells are introduced into a new host, the new host’s immune system recognizes these cells as foreign (or ‘nonself’) and destroys the introduced cells. Therefore, the host’s immune system differentiating between ‘self’ and ‘non-self’ is the reason that cancer is not transmissible. However, if the immune system fails to make this differentiation, cancer can begin to spread between individuals. Since the Tasmanian Devil population has been nearly decimated by several previous population bottlenecks, all devils are very genetically similar. Consequently, the genes that normally confer the ability to differentiate between ‘self’ and ‘non-self’ (e.g. the MHC genes) are so similar between individuals that it is believed that their immune systems can no longer differentiate between tissues from themselves and other devils. Similarly, this is thought to be a cause behind why devils cannot recognize the DFTD cancer, they cannot distinguish the DFTD cancer. Therefore, with the immune system rendered useless against the cancer, DFTD spreads like an infection in an entirely susceptible population (primary research article). Importantly, while MHC genes are very similar between animals, this may not be the only factor that predisposes them to DFTD.

Preventing Extinction with Genomics

The Save the Tasmanian Devil Program was established in 2003 to monitor the devil population, create DFTD diagnostics, establish the impact of the disease in the wild and create an insurance population of animals where there hasn’t been record of the disease (i.e. the northwest area of Tasmania). If the wild devil population goes extinct, the insurance population will play an important role in helping re-establish wild populations in Tasmanian. As of January 2010, the population contained 277 disease-free Tasmanian devils, which currently reside in Australia’s mainland. Since inbreeding and loss of genetic diversity are related to increased extinction probabilities, it is especially important to maintain the highest genetic diversity (e.g. deepest gene pool) as possible to increase the probability that this group survives future population bottlenecks. The Save the Tasmanian Devil program aims to include and manage up to 1,500 devils to maintain the genetic diversity of the species. Our research examines the genetic diversity of the devils across Tasmania using genome sequencing analysis. This work can help guide the selection of the most genetically diverse individuals for the insurance population. Thus, we are helping prevent extinction and guiding the preservation of the Tasmanian Devil through genomics.